First Record of Bat-Pollination in the Species-Rich Genus Tillandsia (Bromeliaceae)
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Annals of Botany 113: 1047–1055, 2014 doi:10.1093/aob/mcu031, available online at www.aob.oxfordjournals.org First record of bat-pollination in the species-rich genus Tillandsia (Bromeliaceae) Pedro Adria´n Aguilar-Rodrı´guez1,*, M. Cristina MacSwiney G.1, Thorsten Kro¨mer1, Jose´ G. Garcı´a-Franco2, Anina Knauer3 and Michael Kessler3 1Centro de Investigaciones Tropicales, Universidad Veracruzana, Casco de la ExHacienda Lucas Martı´n, Privada de Araucarias S/N. Col. Periodistas, C.P. 91019, Xalapa, Veracruz, Me´xico, 2Red de Ecologı´a Funcional, Instituto de Ecologı´a, A.C., Carretera antigua a Coatepec No. 351, El Haya, C.P. 91070, Xalapa, Veracruz, Me´xico and 3Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland * For correspondence. E-mail [email protected] Received: 2 November 2013 Returned for revision: 10 January 2014 Accepted: 12 February 2014 Published electronically: 20 March 2014 Downloaded from † Background and Aims Bromeliaceae is a species-rich neotropical plant family that uses a variety of pollinators, principally vertebrates. Tillandsia is the most diverse genus, and includes more than one-third of all bromeliad species. Within this genus, the majority of species rely on diurnal pollination by hummingbirds; however, the flowers of some Tillandsia species show some characteristics typical for pollination by nocturnal animals, particu- larly bats and moths. In this study an examination is made of the floral and reproductive biology of the epiphytic bro- http://aob.oxfordjournals.org/ meliad Tillandsia macropetala in a fragment of humid montane forest in central Veracruz, Mexico. † Methods The reproductive system of the species, duration of anthesis, production of nectar and floral scent, as well as diurnal and nocturnal floral visitors and their effectiveness in pollination were determined. † Key Results Tillandsia macropetala is a self-compatible species that achieves a higher fruit production through out- crossing. Nectar production is restricted to the night, and only nocturnal visits result in the development of fruits. The most frequent visitor (75 % of visits) and the only pollinatorof this bromeliad (in 96 % of visits) wasthe nectarivorous bat Anoura geoffroyi (Phyllostomidae: Glossophaginae). † Conclusions This is the first report of chiropterophily within the genus Tillandsia. The results on the pollination biology of this bromeliad suggest an ongoing evolutionary switch from pollination by birds or moths to bats. at Cambridge University Library on May 8, 2014 Key words: Tillandsia macropetala, Bromeliaceae, bat-pollination, Anoura geofroyii, bromeliad, chiropterophily, humid montane forest, floral visitors, Mexico, pollinator effectiveness. INTRODUCTION contrasting flowers and diurnal anthesis typical of pollination by hummingbirds (Endress, 1994; Wilmer, 2011). Instead, this The family Bromeliaceae is distributed almost exclusively in the species has a light-green corolla, green bracts and crepuscularan- Neotropics (Benzing, 2000), and 56 % of its species are epiphytic thesis (Kro¨mer et al., 2012). (Zotz, 2013). The family comprises about 3160 species in 50 Tillandsia macropetala was not included (even under its previ- genera, and Tillandsia is the most diverse genus, with more ous name T. viridiflora) inthe classic workof Gardner (1986) about than 670 species, of which 635 are epiphytic (Zotz, 2013). the pollination in Tillandsia, but the related species T. heterophylla Among bromeliads, pollination by vertebrates predominates E. Morren was catalogued as being moth-pollinated. These three over that provided by insects, and most species are pollinated species present particular cases within the genus Tillandsia, by hummingbirds (Kessler and Kro¨mer, 2000; Canela and given their nocturnal anthesis and light-green petals, as seen in Sazima, 2005; Kro¨mer et al., 2006). In some bromeliad genera other bromeliads of the subgenus Pseudoalcantarea (Benzing, (e.g. Guzmania, Pitcairnia and Vriesea), however, syndromes 2000). Whereas Hietz and Hietz-Seifert (1994) suggested that of pollination by insects, birds and bats have evolved independ- sphingid moths could be pollinators of T. viridiflora, Benzing ently (Benzing, 2000). In particular, species of the subfamily (2000) argued based on their floral characteristics that the Tillandsioideae (e.g. Tillandsia, Guzmania and Vriesea)have species of Pseudoalcantarea could be pollinated by bats. on various occasions modified their floral characteristics to The discovery of dilute nectar, rich in hexoses, in T. viridiflora attract a wide range of pollinators (Benzing, 2000). (Kro¨mer et al., 2008), together with other observations also in- The epiphytic bromeliad Tillandsia macropetala Wawra, cluding T. macropetala (T. Kro¨mer and M. C. MacSwiney G., together with T. grandis Schltdl. and T. viridiflora (Beer) pers. obs.), suggests that bats could be their principal pollinators. Baker, belongs to the Mexican species in the Tillandsia viridi- In addition, the helicoiform flowers of T. macropetala stay open flora complex, among which T. macropetala was recently recog- during the morning following anthesis (Kro¨mer et al., 2012), nized as a species distinct from T. viridiflora (Kro¨mer et al., which could enable pollination by both nocturnal and diurnal 2012). It is distributed in central and southern Mexico, in wet visitors (Dar et al., 2006; Ortega-Baes et al., 2011). montane or pine–oak forests at elevations of 1100–2500 m. In In this study, we analysed the floral and reproductive biology contrast to the majority of species of the genus, T. macropetala of T. macropetala. Specifically, (1) the floral visitors that effect- does not present the conspicuously coloured bracts with ively pollinate the flowers were identified, (2) the floral # The Author 2014. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 1048 Aguilar-Rodrı´guez et al. — Bat-pollination in Tillandsia macropetala phenology was described, (3) the production pattern and concen- which is surrounded by a mosaic of anthropized vegetation. For tration of nectar were determined, and the floral scent was logistical reasons, the study in 2012 was conducted in another analysed, and (4) the reproductive system of the bromeliad was fragment 1.2 km from the original site (19831′53.7′′N, assessed. As anthesis in this species begins at dusk and extends 96858′46.8′′W; Fig. 1). This second fragment featured similar into the following day, our primary hypothesis was that vegetation, but was surrounded by fruit trees (Citrus sp., T. macropetala receives both nocturnal and diurnal visits, but Macadamia sp., Musa sp.) and elements of secondary forest. because nocturnal visitors visit the receptive flower first, they will be more important pollinators, accounting for the majority of fruits or seeds. Finally, as suggested by the dilute and Study species hexose-rich nectar, we hypothesized that bats are the main polli- nators of this species. Tillandsia macropetala is an epiphytic bromeliad that is gen- erally found on the trunks and lower parts of its host trees but can also be lithophytic or terrestrial (Kro¨meret al., 2012; Fig. 2A). Its MATERIALS AND METHODS leaves form a stemless tank-type rosette of almost 1.2 m in diam- Study site eter; its inflorescence is 55–83 cm in length and is composed of Downloaded from 3–7 spikes, each with 15–20 flowers. The flowers (Fig. 2B) Fieldworkwas carried outinMarchand April of2011and 2012, in are distichous and erect, actinomorphic and with a subsessile the municipality of Tlalnelhuayocan, in the central region of helicoiform corolla. The petals are light green, strap-shaped, Veracruz State, Mexico. The site has an elevation of 1500– twisted, and 10.7–12.3 cm long and 14–17 mm wide. The light- 1700 m (Mehltreter et al.,2005), with an annual precipitation of green to white stamens are subequal, with free filaments 10.4– 1650 mm and an average temperature of 14 8C(Williams- 11.7 cm long; the anthers are green to green-whitish, curved http://aob.oxfordjournals.org/ Linera, 2002). The predominant vegetation is humid montane and 7.5–8 mm long. The style is free and has a trilobulate forest (Williams-Linera, 2007). Monitoring of T. macropetala stigma (Kro¨mer et al., 2012). phenology was conducted in 2011 in a forest fragment (19831′12.9′′N, 96859′17.9′′W; Fig. 1)wherethedominanttrees were Liquidambar macrophylla Oerst and Quercus spp., and A B c) b) N at Cambridge University Library on May 8, 2014 VERACRUZ MEXICO a) N 3 cm ¢¢ 0 ¢ 19°40 C D 2000 1500 2 1 N ¢¢ 0 XALAPA ¢ 1000 50 μm 19°30 0 2 km F IG.2. Tillandsia macropetala. (A) Individual with inflorescence in its habitat; 97°0¢0¢¢W 96°50¢0¢¢W (B) flower showing the light green petals (a), as well as the extended stamens (b) and style (c); (C) polar view of a pollen grain (phase contrast technique, 25×, F IG. 1. Study area location in the municipality of Tlalnelhuayocan, in central Optovar 2); (D) fruit and seeds, the latter with a plumose appendage. Veracruz, Mexico. Study sites are marked with numbers 1 (2011) and 2 (2012). Photographs: P. A. Aguilar-Rodrı´guez, M. C. MacSwiney G. and A. Knauer. Aguilar-Rodrı´guez et al. — Bat-pollination in Tillandsia macropetala 1049 Phenology and floral anthesis Inc., Tulsa, OK, USA) with a level of significance of P ≤ 0.05. To quantify the self-compatibility of T. macropetala, we calcu- To follow the phenologyof T. macropetala, 17 individualsthat lated the self-compatibility